A shortening muscle is a machine that converts metabolic energy into mechanical work, but, when a muscle is stretched, it acts as a brake, generating a high resistive force at low metabolic cost. The braking action of muscle can be activated with remarkable speed, as when the leg extensor muscles rapidly decelerate the body at the end of a jump. Here we used time-resolved x-ray and mechanical measurements on isolated muscle cells to elucidate the molecular basis of muscle braking and its rapid control. We show that a stretch of only 5 nm between each overlapping set of myosin and actin filaments in a muscle sarcomere is sufficient to double the number of myosin motors attached to actin within a few milliseconds. Each myosin molecule has two motor domains, only one of which is attached to actin during shortening or activation at constant length. A stretch strains the attached motor domain, and we propose that combined steric and mechanical coupling between the two domains promotes attachment of the second motor domain. This mechanism allows skeletal muscle to resist external stretch without increasing the force per motor and provides an answer to the longstanding question of the functional role of the dimeric structure of muscle myosin.

Skeletal muscle resists stretch by rapid binding of the second motor domain of myosin to actin / E. BRUNELLO; M. RECONDITI; R. ELANGOVAN; M. LINARI; Y.-B. SUN; T. NARAYANAN; P. PANINE; G. PIAZZESI; M. IRVING; V. LOMBARDI. - In: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. - ISSN 0027-8424. - STAMPA. - 104:(2007), pp. 20114-20119. [10.1073/pnas.0707626104]

Skeletal muscle resists stretch by rapid binding of the second motor domain of myosin to actin

BRUNELLO, ELISABETTA;RECONDITI, MASSIMO;ELANGOVAN, RAVI KRISHNAN;LINARI, MARCO;PIAZZESI, GABRIELLA;LOMBARDI, VINCENZO
2007

Abstract

A shortening muscle is a machine that converts metabolic energy into mechanical work, but, when a muscle is stretched, it acts as a brake, generating a high resistive force at low metabolic cost. The braking action of muscle can be activated with remarkable speed, as when the leg extensor muscles rapidly decelerate the body at the end of a jump. Here we used time-resolved x-ray and mechanical measurements on isolated muscle cells to elucidate the molecular basis of muscle braking and its rapid control. We show that a stretch of only 5 nm between each overlapping set of myosin and actin filaments in a muscle sarcomere is sufficient to double the number of myosin motors attached to actin within a few milliseconds. Each myosin molecule has two motor domains, only one of which is attached to actin during shortening or activation at constant length. A stretch strains the attached motor domain, and we propose that combined steric and mechanical coupling between the two domains promotes attachment of the second motor domain. This mechanism allows skeletal muscle to resist external stretch without increasing the force per motor and provides an answer to the longstanding question of the functional role of the dimeric structure of muscle myosin.
2007
104
20114
20119
E. BRUNELLO; M. RECONDITI; R. ELANGOVAN; M. LINARI; Y.-B. SUN; T. NARAYANAN; P. PANINE; G. PIAZZESI; M. IRVING; V. LOMBARDI
File in questo prodotto:
File Dimensione Formato  
Brunello et al 2007.pdf

Accesso chiuso

Tipologia: Versione finale referata (Postprint, Accepted manuscript)
Licenza: DRM non definito
Dimensione 1.05 MB
Formato Adobe PDF
1.05 MB Adobe PDF   Richiedi una copia
Supporting Information — PNAS2007.mht

Accesso chiuso

Tipologia: Versione finale referata (Postprint, Accepted manuscript)
Licenza: DRM non definito
Dimensione 301.11 kB
Formato Unknown
301.11 kB Unknown   Richiedi una copia

I documenti in FLORE sono protetti da copyright e tutti i diritti sono riservati, salvo diversa indicazione.

Utilizza questo identificatore per citare o creare un link a questa risorsa: https://hdl.handle.net/2158/255565
Citazioni
  • ???jsp.display-item.citation.pmc??? ND
  • Scopus 91
  • ???jsp.display-item.citation.isi??? 79
social impact